Extensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome in<i>Drosophila pseudoobscura</i>

Fuller, Zachary L.; Koury, Spencer; Leonard, Christopher J.; Young, Randee E.; Ikegami, Kobe; Westlake, Jonathan; Richards, Stephen; Schaeffer, Stephen W.; Phadnis, Nitin

doi:10.1534/genetics.120.303460

Cited by 20 publications

(40 citation statements)

References 180 publications

(250 reference statements)

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“…In fact, all markers within haploblock HB27a (in QTL-2 ) experienced segregation distortion in the yellow QTL mapping population. Segregation distortion is common in mapping studies, can be associated with chromosomal inversions (Fuller et al, 2020; X. Li, Wang, Wei, & Brummer, 2011), and is often caused by meiotic drive (Lyttle, 1993).…”

Section: Discussionmentioning

confidence: 99%

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

Prapas

Scalone

Lee

et al. 2022

Preprint

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Biological invasions offer a unique opportunity to investigate evolution over contemporary time-scales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species' invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high-density linkage map (4,493 SNPs) and paired this with phenotypic data from an F2 mapping population (n=336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger and more tightly-linked alleles should underlie rapid local adaptation during invasion, particularly when divergently-adapting populations experience high-levels of gene flow.

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Section: Discussionmentioning

confidence: 99%

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

Prapas

Scalone

Lee

et al. 2022

Preprint

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“…Inversions with a large effect on complex multitrait phenotypes, such as lifehistory, behaviour, and colour patterns, confirm that arrangements can behave as haplotypes of a "supergene", linking together combinations of alleles within each arrangement (Joron et al 2011;Schwander et al 2014;Kirubakaran et al 2016;Wellenreuther and Bernatchez 2018;Yan et al 2020). Inversions are also notable for their associations with segregation distorters, involving epistatic selection which favours linkage between coadapted alleles at interacting loci (Sturtevant and Dobzhansky 1936;Fuller et al 2020). Likewise, covariation between inversion frequencies and environmental variables, whether spatial, temporal or experimental, (Dobzhansky 1948;Schaeffer 2008;Kapun et al 2016;Kirubakaran et al 2016;Faria et al 2019;Kapun and Flatt 2019;Huang and Rieseberg 2020) is consistent with selection for the suppression of recombination between locally adaptive loci (Kirkpatrick and Barton 2006;Charlesworth and Barton 2018) and/or coadaptive epistatic interactions between loci (Dobzhansky and Dobzhansky 1970;Charlesworth and Charlesworth 1973).…”

Section: Introductionmentioning

confidence: 99%

Locally adaptive inversions modulate genetic variation at different geographic scales in a seaweed fly

Mérot¹,

Berdan

Cayuela

et al. 2020

Preprint

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Across a species range, spatially-varying environments can drive the evolution of local adaptation. Multiples sources of environmental heterogeneity, at small and large scales, draw complex landscapes of selection which may challenge adaptation, particularly when gene flow is high. Because linkage opposes gene flow but also limits the efficiency of natural selection by contrasting pressures, the key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants like chromosomal inversions are important recombination modifiers that form massive co-segregating genomic blocks linking together alleles at numerous genes. In this study, we investigate the influence of chromosomal rearrangements on genetic variation to ask how their contribution to adaptation with gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient of 10° of latitude, a salinity gradient and across a range of heterogeneous, patchy habitats. We assembled a high-quality genome to analyse 1,446 low-coverage whole-genome sequences, and we found large non-recombining genomic regions, including putative inversions. In contrast to the collinear regions depicting extensive gene flow, inversions and low-recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. Those genomic regions were disproportionately involved in associations with environmental factors and adaptive phenotypes, albeit with contrasting patterns between the different recombination modifiers. Altogether, our results highlight the importance of recombination in shaping the selection-migration balance and show that a set of several inversions behave as modular cassettes facilitating adaptation to environmental heterogeneity at local and large scales.

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“…Inversions with a large effect on complex multitrait phenotypes, such as life-history, behavior, and color patterns, confirm that arrangements can behave as haplotypes of a “supergene,” linking together combinations of alleles within each arrangement ( Joron et al 2011 ; Schwander et al 2014 ; Kirubakaran et al 2016 ; Wellenreuther and Bernatchez 2018 ; Yan et al 2020 ). Inversions are also notable for their associations with segregation distorters, involving epistatic selection which favors linkage between coadapted alleles at interacting loci ( Sturtevant and Dobzhansky 1936 ; Fuller et al 2020 ). Likewise, covariation between inversion frequencies and environmental variables, whether spatial, temporal, or experimental ( Dobzhansky 1948 ; Schaeffer 2008 ; Kapun et al 2016 ; Kirubakaran et al 2016 ; Faria et al 2019 ; Kapun and Flatt 2019 ; Huang and Rieseberg 2020 ) is consistent with selection for the suppression of recombination between locally adaptive loci ( Kirkpatrick and Barton 2006 ; Charlesworth and Barton 2018 ) and/or coadaptive epistatic interactions between loci ( Dobzhansky and Dobzhansky 1970 ; Charlesworth and Charlesworth 1973 ).…”

Section: Introductionmentioning

confidence: 99%

Locally Adaptive Inversions Modulate Genetic Variation at Different Geographic Scales in a Seaweed Fly

Mérot

Berdan

Cayuela

et al. 2021

Molecular Biology and Evolution

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Across a species range, multiple sources of environmental heterogeneity, at both small and large scales, create complex landscapes of selection, which may challenge adaptation, particularly when gene flow is high. One key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants, like chromosomal inversions, reduce recombination, increasing linkage disequilibrium among loci at a potentially massive scale. In this study, we examined how chromosomal inversions shape genetic variation across a species range, and ask how their contribution to adaptation in the face of gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient stretching across 10° of latitude, a salinity gradient and a range of heterogeneous, patchy habitats. We generated a chromosome-level genome assembly to analyse 1,446 low-coverage whole genomes collected along those gradients. We found several large non-recombining genomic regions, including putative inversions. In contrast to the collinear regions, inversions and low recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. These genomic regions were associated with environmental factors and adaptive phenotypes, albeit with contrasting patterns. Altogether, our results highlight the importance of recombination in shaping adaptation to environmental heterogeneity at local and large scales.

show abstract

Extensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome inDrosophila pseudoobscura

Cited by 20 publications

References 180 publications

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

Locally adaptive inversions modulate genetic variation at different geographic scales in a seaweed fly

Locally Adaptive Inversions Modulate Genetic Variation at Different Geographic Scales in a Seaweed Fly

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